Differences exist between the gastric mucosa in adults and foals. The squamous gastric epithelium increases in cell depth and keratinisation over the first few weeks of life (Murray and Mahaffey, 1993). This is thought in part to be related to increasing exposure to gastric acid in addition to growth factors present in milk. The gastric pH level of neonatal foals is slightly higher than more mature individuals. The ventral gastric pH level of newborn foals is approximately 4 and decreases to a more adult type pH level of around 2 by 3 days of age (Baker, 1993). There is significant daily variation in the gastric pH level in healthy foals. Milk ingestion has an important alkalinising effect and the pH level drops during sleep (Sanchez et al, 1998). The typical pH range is between 0.8 and 6, but the majority of healthy foals have an acidic pH similar to adult values by a week of age. In contrast, sick neonates have different gastric pH profiles. Many sick neonates have a consistently alkaline pH (Sanchez et al, 2001). The ability to produce an acidic gastric pH seems to have an association with survival. In one study 77% of foals with a gastric pH less than 5 (even transiently) survived compared with only 20% of foals with alkaline pH (Sanchez et al, 2001).
Risk factors
The risk factors for equine gastric ulcer syndrome (EGUS) in foals vary depending on foal age. In very young neonatal foals, excess exposure to acid is probably not a major risk factor as many foals have an alkaline gastric pH. In these foals abnormalities in perfusion are probably much more important. Specific studies evaluating gastrointestinal perfusion in neonatal foals are not available, but the association between poor perfusion and non-survival using lactate as a marker is well recognised (Borchers et al, 2013). Lack of milk ingestion is also important as this may effect stimulation of local factors and mucosal health. In older foals the risk factors for EGUS are probably much more similar to adult horses. Excess exposure to acid is likely more important and other factors, such as stress and anorexia, are likely to be as important as abnormalities in perfusion. Stress and weaning have both been shown to be associated with the presence of EGUS (Furr et al, 1992; Vondran et al, 2016). The use of non-steroidal anti-inflammatory drugs (NSAIDs) such as equipalazone has also been shown to be associated with EGUS (Geor et al, 1989).
Prevalence of equine gastric disease in foals
The reported prevalence of EGUS in foals varies depending on the underlying population and the sampling protocols. Murray et al reported that 51% of healthy thoroughbred foals less than 3 months of age had EGUS (Murray et al, 1990). Ulcers in this study were predominantly squamous, although full evaluation of the glandular mucosa was not performed in all foals. A large necropsy study of 691 foals that did not survive for a variety of reasons reported a lower prevalence of ulceration with 22% of foals having gastric or duodenal lesions (Elfenbein and Sanchez, 2012). The presence of gastrointestinal disease, especially diarrhoea, appears to be a major risk factor for an increased incidence of EGUS. Disease is also more commonly identified in older foals rather than neonates.
Clinical signs of equine gastric ulcer syndrome in foals
The classic reported clinical signs of EGUS in foals include colic, bruxism and hypersalivation; however, clinical signs are often much less specific and usually include general ill-thrift, mild anorexia and decreased weight gain. In the author's experience, a mild but persistent increase in plasma fibrinogen concentration is often seen. Foals that have significant duodenal disease usually have much more profound clinical signs. These usually include severe hypersalivation and bruxism (often due to significant oesophageal ulceration), weight loss, anorexia, persistent colic and gastric reflux. Unfortunately, some foals with EGUS do not demonstrate any clinical signs and a peracute presentation can occur following rupture of a gastric ulcer (Figure 1).
Diagnosis
Diagnosis requires gastroscopy (Figure 2). This is carried out in a similar way to in adult horses. In a young neonate (less than a month of age) only a short period of fasting is required (2 hours). This is usually best carried out by the use of a muzzle to prevent nursing. The duration of fasting that is required increases with the age of foal and most foals greater than 1 month of age will require 6–12 hours of fasting to allow adequate visualisation. In foals with significant duodenal disease prolonged fasting (>24 hours) may be required. This may be detrimental to the foal and consequently visualisation of the duodenal mucosa is not always possible in these cases. Minimal complications have been reported associated with gastroscopy. Light sedation is usually necessary and a combination of a low dose of an alpha-2 agonist such as xylazine with butorphanol is usually effective. A 2 m scope has an adequate length and a small gag should still be used to prevent the risk of scope injury from retroflexion.
Additional tools that can be useful for the diagnosis of duodenal disease include abdominal ultrasound, which may reveal gastric distension or an increased duodenal wall thickness (Figure 3). Contrast radiography can also be used to evaluate gastric emptying; 10 ml/kg of liquid barium is adminstered via nasogastric tube and abdominal radiographs taken every 15 minutes. Barium should be visible in the small intestine within 15 minutes. A delay of greater than 30–45 minutes confirms delayed gastric emptying (Figure 4).
Treatment
A treatment plan for foals should consider management/reduction of any potential risk factors in addition to the use of medication. There are few studies comparing the efficacy of different medications or the pharmacokinetics and pharmacodynamics of commonly used medications in foals, so some extrapolation from adult horses is needed.
Omeprazole is generally considered the first-line treatment for EGUS in foals. This drug is well absorbed when given orally to healthy foals and causes effective prolonged acid suppression after a single dose (Sanchez et al, 2004). Pharmacokinetics have only been evaluated at the 4 mg/kg dose of enteric coated formula and consequently this dose is usually recommended; however, it is likely that lower doses may also be effective based on the good bioavailability in foals. The efficacy of omeprazole for treatment of EGUS in foals has not been extensively investigated. A field study by MacAllister et al (1999) showed a positive response to treatment in a sub-group of foals; however, no studies have evaluated the efficacy of oral omeprazole for the treatment of glandular disease in foals. Extrapolation from adults might suggest that oral omeprazole is unlikely to be effective, but in younger foals that have reliable drug absorption and prolonged acid suppression the drug may be more effective alone than in adult horses. Oral omeprazole has also been shown to cause reliable acid suppression in sick foals (Javsicas and Sanchez, 2008). Injectable omeprazole has anecdotally been used in foals with good clinical effect, but no studies have evaluated its use and this medication is not licensed in foals.
Acid suppression can also be achieved using histamine receptor antagonists; however, these medications generally cause less reliable acid suppression. Intravenous ranitidine has been shown to increase gastric pH in healthy foals for 4 hours, but the effect in critically ill foals is variable and less reliable (Sanchez et al, 1998; 2001). Oral ranitidine can increase gastric pH for 6 hours in healthy foals.
Misoprostol is now considered a first-line treatment for glandular disease in adult horses (Varley et al, 2019). No studies have evaluated its use in foals, but anecdotally the drug can be used at the adult dose (5 ug/kg per os twice daily) without adverse effects. Sucralfate is a mucosal adherent. Beneficial effects should include ulcer binding, promotion of mucosal blood flow and increased production of bicarbonate, mucus and prostaglandin. This drug is widely used, but there is sparse literature supporting it use. In one study, sucralfate showed no benefit in healing of glandular ulceration compared with the use of corn oil (Borne and MacAllister, 1993). However, a study evaluating the use of phenylbutazone in foals showed that when phenylbutazone was combined with oral sucralfate, adverse side effects were much reduced (Geor et al, 1989). Sucralfate may be beneficial in any foal with evidence of oesophageal lesions or clinical signs suggestive of severe ulceration (hypersalivation, bruxism etc).
Treatment of foals with duodenal disease or delayed gastric emptying is more challenging. Medical treatment with intravenous fluids, nutritional support, pro-kinetics and general nursing care is often needed. In some foals, once the inflammation has subsided gastric emptying improves and clinical recovery can occur. If the disease causes more severe structural changes with stenosis of the pylorus or duodenal stricture, then surgical treatment may be necessary. Gastrojejunostomy can be used to bypass the diseased gastric outflow. The reported success of this procedure is a 50% chance of long-term success with return to racing (Coleman et al, 2009).
Treatment/prevention of EGUS should also consider other factors. Maximising perfusion should be considered a major priority in critically ill foals as this is likely to help maintain gastric perfusion. This is likely to be much more important than the use of medication. Ensuring adequate milk intake should also be attempted when possible. This may necessitate placement of an indwelling nasogastric tube to provide mare's milk in a foal that cannot nurse from the mare, or provide additional milk feeding to foals that are not nursing adequately. Milk helps alkalinise the gastric pH and should help stimulate local blood flow, growth factors etc. In older foals ensuring access to good quality turnout and forage is essential. Concentrate feed should be fed in small amounts and should be low in rapidly digestible carbohydrates. It is also important to try to minimise stress. This can be difficult, but consideration should be given to ensuring stable social groups, maximising turnout and minimising stabling. Additional efforts should be made at weaning to try to make this as stress free as possible.
In general it is useful to try to minimise use of NSAIDs. This is especially important in neonatal foals and in foals with perfusion abnormalities (such as foals with diarrhoea). However, NSAIDs can be very useful in foals to provide anti-inflammatory effects and analgesia, especially in foals with orthopaedic disease. The duration of treatment should be kept as short as possible, but consideration should also be given to the type of NSAID used. Phenylbutazone and flunixin both induce gastrointestinal ulceration. Newer generation NSAIDs which have more COX-2 selectivity, should be used in preference. Meloxicam provides good analgesia in foals and has been shown to cause minimal adverse effects (Raidal et al, 2013).
There is a great deal of pressure in veterinary practice to use anti-ulcer medications prophylactically to prevent EGUS. This is mainly driven by the occasional loss of a foal because of gastric perforation. However, there is little evidence in the literature that prophylaxis is very effective. In the large post-mortem study carried out by Elfenbein and Sanchez (2012) the prevalence of EGUS was similar in foals with and without ulcer prophylaxis. A large multicentre study of hospitalised foals (Furr et al, 2012) also showed that the presence of EGUS in foals was similar between treated and untreated foals. However, based on the evidence that the risk of EGUS is higher in certain groups of foals, then treatment is probably warranted in certain groups. The groups that may benefit from treatment include foals with diarrhoea or other intestinal disease, foals receiving treatment with NSAIDs and foals experiencing greater than normal amounts of stress. Older foals in general are more likely to have EGUS. When prophylaxis is considered logical then oral omeprazole is probably the most logical choice. Theoretically, misoprostol could be considered in foals receiving NSAIDs as this may minimise some of the adverse effects.
One additional consideration in ill neonatal foals is the suggestion that an alkaline gastric pH is associated with an increased risk of mortality. In critically ill human neonates there is some evidence that the use of acid suppressive medication can increase the risk of bacterial colonisation of the intestinal tract with subsequent sepsis from bacterial translocation. This has not been shown in neonatal foals, but use of anti-ulcer medication has been suggested to increase the risk of diarrhoea in hospitalised foals (Furr et al, 2012).
Conclusion
EGUS is a common condition in foals and can be challenging to identify and treat. In neonatal foals, treatment should focus on maximising perfusion and milk intake. Acid suppressive medication is probably not indicated for the majority of foals in this age group and may be associated with potentially detrimental effects. There may be some rationale for the use of sucralfate in this age of foals, as this may have beneficial effects on the gastric mucosa. In older foals, EGUS is more prevalent and acid suppressive medication is more logical. Foals that fall into high risk groups (diarrhoea, NSAID use, stress) should be treated with oral omeprazole as the first-line drug of choice. Efforts should also be made to minimise risk factors. Irrespective of the age of foal, treatment is indicated if a foal shows clinical signs suggestive of EGUS. In these foals the combination of omeprazole and sucralfate may be logical.
KEY POINTS
- Equine gastric ulcer syndrome (EGUS) is a common problem in foals.
- The underlying causes and risk factors change with increasing foal age.
- Clinical signs of EGUS include hypersalivation, bruxism and colic. However, many foals with EGUS have no obvious clinical signs or just show signs of decreased weight gain and mild lethargy.
- Diagnosis relies on gastroscopic examination.
- A number of medications can be used to treat EGUS in foals but omeprazole and sucralfate are most commonly used.